Distribution modelling and statistical phylogeography: an integrative framework for generating and testing alternative biogeographical hypotheses

Statistical phylogeographic studies contribute to our understanding of the factors that influence population divergence and speciation, and that ultimately generate biogeographical patterns. The use of coalescent modelling for analyses of genetic data provides a framework for statistically testing alternative hypotheses about the timing and pattern of divergence. However, the extent to which such approaches contribute to our understanding of biogeography depends on how well the alternative hypotheses chosen capture relevant aspects of species histories. New modelling techniques, which explicitly incorporate spatio-geographic data external to the gene trees themselves, provide a means for generating realistic phylogeographic hypotheses, even for taxa without a detailed fossil record. Here we illustrate how two such techniques – species distribution modelling and its historical extension, palaeodistribution modelling – in conjunction with coalescent simulations can be used to generate and test alternative hypotheses. In doing so, we highlight a few key studies that have creatively integrated both historical geographic and genetic data and argue for the wider incorporation of such explicit integrations in biogeographical studies.     

Paleodistributions and comparative molecular phylogeography of leafcutter ants (Atta spp.) provide new insight into the origins of Amazonian diversity

The evolutionary basis for high species diversity in tropical regions of the world remains unresolved. Much research has focused on the biogeography of speciation in the Amazon Basin, which harbors the greatest diversity of terrestrial life. The leading hypotheses on allopatric diversification of Amazonian taxa are the Pleistocene refugia, marine incursion, and riverine barrier hypotheses. Recent advances in the fields of phylogeography and species-distribution modeling permit a modern re-evaluation of these hypotheses. Our approach combines comparative, molecular phylogeographic analyses using mitochondrial DNA sequence data with paleodistribution modeling of species ranges at the last glacial maximum (LGM) to test these hypotheses for three co-distributed species of leafcutter ants (Atta spp.). The cumulative results of all tests reject every prediction of the riverine barrier hypothesis, but are unable to reject several predictions of the Pleistocene refugia and marine incursion hypotheses. Coalescent dating analyses suggest that population structure formed recently (Pleistocene-Pliocene), but are unable to reject the possibility that Miocene events may be responsible for structuring populations in two of the three species examined. The available data therefore suggest that either marine incursions in the Miocene or climate changes during the Pleistocene--or both--have shaped the population structure of the three species examined. Our results also reconceptualize the traditional Pleistocene refugia hypothesis, and offer a novel framework for future research into the area.     

Comparative phylogeography as an integrative approach to historical biogeography

Phylogeography has become a powerful approach for elucidating contemporary geographical patterns of evolutionary subdivision within species and species complexes. A recent extension of this approach is the comparison of phylogeographic patterns of multiple co-distributed taxonomic groups, or 'comparative phylogeography.' Recent comparative phylogeographic studies have revealed pervasive and previously unrecognized biogeographic patterns which suggest that vicariance has played a more important role in the historical development of modern biotic assemblages than current taxonomy would indicate. Despite the utility of comparative phylogeography for uncovering such 'cryptic vicariance', this approach has yet to be embraced by some researchers as a valuable complement to other approaches to historical biogeography. We address here some of the common misconceptions surrounding comparative phylogeography, provide an example of this approach based on the boreal mammal fauna of North America, and argue that together with other approaches, comparative phylogeography can contribute importantly to our understanding of the relationship between earth history and biotic diversification.     

鸟类分子系统地理学研究进展

分子系统地理学是当代生物地理学的重要分支,是以分子生物学方法重建种内和种上水平的系统发育关系,阐释进化历史,并通过分析近缘生物类群的系统发育关系与其空间和时间分布格局间的相关性构建生物区系历史的研究,是分子生物学与生物地理学结合的产物。中性进化学说和溯祖理论分析的建立,以及线粒体DNA和微卫星标记等分子遗传标记的应用,为分子系统地理学研究的开展提供了理论和实践基础。近年来,分子系统地理方法在鸟类学研究中的应用揭示了许多不同于传统认知的发现,为准确而深入的了解鸟类分子系统地理格局的差异和不同类群的起源中心提供了新颖的证据。目前的研究多从隔离分化说和扩散说的角度对鸟类分子系统地理格局的成因进行分析,而迁徙行为不同对鸟类系统地理格局的影响为成因的解释提供了新的角度。结合区域特点的比较分子系统地理研究,在更广泛的地域和更多类群中开展研究是我国鸟类分子系统地理研究的方向。此外,展望了第二代测序技术对分子生态生物地理研究具有的潜在促进作用。     

Congruence, consensus, and the comparative phylogeography of codistributed species in California

Comparative phylogeography has emerged as a means of understanding the spatial patterns of genetic divergence of codistributed species. However, researchers are often frustrated because of the lack of appropriate statistical tests to assess concordancy of multiple phylogeographic trees. We develop a method for testing congruence across multiple species and synthesizing the data into a regional supertree. Nine phylogeographic data sets of species with different life histories and ecologies were statistically compared using maximum agreement subtrees (MAST) and showed a high degree of concordancy. A supertree combining the different phylogeographic trees was then computed using matrix representation with parsimony, and the groups defined by this supertree were tested against climatic data to investigate a potential mechanism driving divergence. Our data suggest that species and genetic lineages in California are shaped by climatic regimes. The supertree method in combination with MAST represents a new approach to test congruence hypotheses and detect common geographic signals in comparative phylogeography.     

Comparative phylogeography of trans‐Andean freshwater fishes based on genome‐wide nuclear and mitochondrial markers

The Neotropical region represents one of the greatest biodiversity hot spots on earth. Despite its unparalleled biodiversity, regional comparative phylogeographic studies are still scarce, with most focusing on model clades (e.g. birds) and typically examining a handful of loci. Here, we apply a genome‐wide comparative phylogeographic approach to test hypotheses of codiversification of freshwater fishes in the trans‐Andean region. Using target capture methods, we examined exon data for over 1,000 loci combined with complete mitochondrial genomes to study the phylogeographic history of five primary fish species (>150 individuals) collected from eight major river basins in Northwestern South America and Lower Central America. To assess their patterns of genetic structure, we inferred genealogical concordance taking into account all major aspects of phylogeography (within loci, across multiple genes, across species and among biogeographic provinces). Based on phylogeographic concordance factors, we tested four a priori biogeographic hypotheses, finding support for three of them and uncovering a novel, unexpected pattern of codiversification. The four emerging inter‐riverine patterns are as follows: (a) Tuira + Atrato, (b) Ranchería + Catatumbo, (c) Magdalena system and (d) Sinú + Atrato. These patterns are interpreted as shared responses to the complex uplifting and orogenic processes that modified or sundered watersheds, allowing codiversification and speciation over geological time. We also find evidence of cryptic speciation in one of the species examined and instances of mitochondrial introgression in others. These results help further our knowledge of the historical geographic factors shaping the outstanding biodiversity of the Neotropics.     

INTRASPECIFIC PHYLOGEOGRAPHY ACROSS THE POINT CONCEPTION BIOGEOGRAPHIC BOUNDARY

Recent studies of intraspecific phylogeography have suggested that the geographic location of genetic discontinuities, or phylogeographic breaks, may frequently coincide with biogeographic boundaries. The concordance is hypothesized to reflect similarity in the processes governing species boundaries and intraspecific lineage boundaries. This concordance has not, however, been widely tested. In the case of the Point Conception biogeographic boundary between the Oregonian and Californian marine biotas, only the supralittoral copepod Tigriopus californicus has been found to have a coincident phylogeographic break. Here I show that the apparent relationship between this break and Point Conception was, in fact, an artifact of insufficient geographic sampling. Mitochondrial DNA analyses of T. californicus populations between Morro Bay and San Diego reveal at least five equally deep phylogeographic breaks in the region (where only one biogeographic boundary is recognized). Limited nuclear DNA sequence data and allozyme data also support the occurrence of multiple genetic discontinuities along this geographic range. Lack of one-to-one correspondence between intraspecific phylogeography and biogeographic boundaries indicates that the processes affecting the genetic differentiation of populations of T. californicus differ from those responsible for determining species distributional limits at the Point Conception biogeographic boundary. A review of genetic data from other species also fails to provide evidence for concordance of biogeography and intraspecific phylogeography across Point Conception. I suggest that the concordance of phylogeography with biogeography will only be pronounced where the biogeographic boundary separates biotas that are phylogenetically related. The numerous cases of interspecific hybrid zones in the region of Cape Canaveral, for example, indicate that many sister-species pairs occur across this biogeographic boundary. Such hybrid zones are not common at Point Conception, and there appears to be no cases of intraspecific phylogeographic breaks associated with this well-recognized biogeographic boundary.     

Evaluating mechanisms of diversification in a Guineo‐Congolian tropical forest frog using demographic model selection

The accumulation of biodiversity in tropical forests can occur through multiple allopatric and parapatric models of diversification, including forest refugia, riverine barriers and ecological gradients. Considerable debate surrounds the major diversification process, particularly in the West African Lower Guinea forests, which contain a complex geographic arrangement of topographic features and historical refugia. We used genomic data to investigate alternative mechanisms of diversification in the Gaboon forest frog, Scotobleps gabonicus, by first identifying population structure and then performing demographic model selection and spatially explicit analyses. We found that a majority of population divergences are best explained by allopatric models consistent with the forest refugia hypothesis and involve divergence in isolation with subsequent expansion and gene flow. These population divergences occurred simultaneously and conform to predictions based on climatically stable regions inferred through ecological niche modelling. Although forest refugia played a prominent role in the intraspecific diversification of S. gabonicus, we also find evidence for potential interactions between landscape features and historical refugia, including major rivers and elevational barriers such as the Cameroonian Volcanic Line. We outline the advantages of using genomewide variation in a model‐testing framework to distinguish between alternative allopatric hypotheses, and the pitfalls of limited geographic and molecular sampling. Although phylogeographic patterns are often species‐specific and related to life‐history traits, additional comparative studies incorporating genomic data are necessary for separating shared historical processes from idiosyncratic responses to environmental, climatic and geological influences on diversification.     

History, ocean channels, and distance determine phylogeographic patterns in three widespread Philippine fruit bats (Pteropodidae)

The comparative phylogeography of widespread, codistributed species provides unique insights into regional biodiversity and diversification patterns. I used partial DNA sequences of the mitochondrial genes ND2 and cyt b to investigate phylogeographic structure in three widespread Philippine fruit bats. Ptenochirus jagori is endemic to the oceanic region of the Philippines and is most abundant in lowland primary forest. Macroglossus minimus and Cynopterus brachyotis are most common in disturbed and open habitats and are not endemic. In all three, genetic differentiation is present at multiple spatial scales and is associated to some degree with Pleistocene landbridge island groups. In P. jagori and C. brachyotis, genetic distance is correlated with geographic distance; in C. brachyotis and M. minimus, it is correlated with the sea-crossing distance between islands. P. jagori has the least overall genetic structure of these three species, whereas C. brachyotis and M. minimus have more geographic association among haplotypes, suggesting that phylogeographic patterns are linked to ecology and habitat preference. However, contrary to expectation, the two widespread, disturbed habitat species have more structure than the endemic species. Mismatch distributions suggest rapid changes in effective population size in C. brachyotis and P. jagori, whereas M. minimus appears to be demographically more stable. Geologic and geographic history are important in structuring variation, and phylogeographic patterns are the result of dynamic long-term processes rather than simply reflecting current conditions.     

Miniaturizing landscapes to understand species distributions

Species’ geographic distributions shape global patterns of biodiversity and therefore have long been of interest to ecology and conservation. Theory has generated valuable hypotheses about how landscape structure, dispersal, biotic interactions and evolution shape range dynamics, but most predictions have not been tested on real organisms because key variables are difficult to isolate, replicate or manipulate in natural ecosystems. An exciting and rapidly emerging approach is to extend classical microcosm and mesocosm systems to create experimental ‘micro-landscapes’. By enabling researchers to manipulate geographic features of interest, replicate landscapes, control colonization and follow dynamics across evolutionary timescales, micro-landscapes allow explicit tests of the ecological and evolutionary underpinnings of species distributions. Here we review the micro-landscape systems being used to advance biogeography, the major insights they have generated thus far, and the features that limit their application to some scenarios. We end by highlighting important questions about species’ biogeography that are ripe for testing with experimental micro-landscapes, particularly those of immediate concern given rapid global change, such as range contractions and constraints to range expansion.     

分子系统地理学及其应用

分子系统地理学是20世纪70年代中期伴随着对线粒体DNA的认识而开始酝酿发展的,本文回顾了该学科自诞生以来的发展简史,阐述了其研究内容,着重从3个方面介绍了该领域在其它相关学科中的研究进展,总结了该学科存在的问题,并提出重点应解决的3个问题：1）将细胞器基因与遗传信息更为丰富的核基因相结合;2）合生理论在非平衡种群中的发展应用;3）提高对分化时间估计的精确性。     

The role of physical barriers in the location of avian suture zones in the Guiana Shield, northern Amazonia

Suture zones represent natural forums in which to examine the role of geography and ecology in the speciation process. Here, we conduct a comparative analysis designed to investigate the location of avian phylogeographic breaks and contact zones in the Guiana Shield, northern Amazonia. We use distributional and genetic data from 78 pairs of avian taxa to address whether phylogeographic breaks and contact zones are associated with contemporary landscape features. Using spatially explicit statistical models, we found that phylogeographic breaks and contact zones are not randomly distributed throughout the landscape. In general, geographic breaks cluster along physical barriers (rivers, nonforested habitats, and small mountain ranges), whereas contact zones aggregate where these barriers either break down or are easier to overcome, such as around rivers' headwaters. Our results indicate that although major Amazonian rivers are often key determinants of taxon boundaries, the "riverine barrier effect" is a synergistic consequence of the wide lower reaches of some rivers, coupled with nonriverine landscape features at the headwaters. Our data suggest that ancestral refugia are not necessary to explain current distribution patterns and that pairs of codistributed taxa do not seem to be the result of simultaneous diversification processes.     

Phylogeography and biogeography of the lower Central American Neotropics: diversification between two continents and between two seas

Lower Central America (LCA) provides a geologically complex and dynamic, richly biodiverse model for studying the recent assembly and diversification of a Neotropical biota. Here, we review the growing literature of LCA phylogeography studies and their contribution to understanding the origins, assembly, and diversification of the LCA biota against the backdrop of regional geologic and climatic history, and previous biogeographical inquiry. Studies to date reveal that phylogeographical signal within taxa of differing distributions reflects a diversity of patterns and processes rivalling the complexities of LCA landscapes themselves. Even so, phylogeography is providing novel insights into regional diversification (e.g. cryptic lineage divergences), and general evolutionary patterns are emerging. Congruent multi‐taxon phylogeographic breaks are found across the Nicaraguan depression, Chorotega volcanic front, western and central Panama, and the Darién isthmus, indicating that a potentially shared history of responses to regional‐scale (e.g. geological) processes has shaped the genetic diversity of LCA communities. By contrast, other species show unique demographic histories in response to overriding historical events, including no phylogeographic structure at all. These low‐structure or incongruent patterns provide some evidence for a role of local, ecological factors (e.g. long‐distance dispersal and gene flow in plants and bats) in shaping LCA communities. Temporally, comparative phylogeographical structuring reflects Pliocene–Pleistocene dispersal and vicariance events consistent with the timeline of emergence of the LCA isthmus and its major physiographic features, e.g. cordilleras. We emphasise the need to improve biogeographic inferences in LCA through in‐depth comparative phylogeography projects capitalising on the latest statistical phylogeographical methods. While meeting the challenges of reconstructing the biogeographical history of this complex region, phylogeographers should also take up the critical service to society of applying their work to the conservation of its fascinating biodiversity.     

Driven by the West Wind Drift? A synthesis of southern temperate marine biogeography,with new directions for dispersalism

Aim Twentieth century biogeographers developed intriguing hypotheses involving West Wind Drift dispersal of Southern Hemisphere biota, but such models were largely abandoned in favour of vicariance following the development of plate tectonic theory. Here I present a synthesis of southern temperate marine biogeography, and suggest some new directions for phylogeographic research. Location The southern continents, formerly contiguous components of Gondwana, are now linked only by ocean currents driven by the West Wind Drift. Methods While vicariance theory certainly facilitates the development of testable hypotheses, it does not necessarily follow that vicariance explains much of contemporary southern marine biogeography. To overcome the limitations of narratives that simply assume vicariance or dispersal, it is essential for analyses to test biogeographic hypotheses by incorporating genetic, ecological and geological data. Results Recent molecular studies have provided strong evidence for dispersal, but relatively little evidence for the biogeographic role of plate tectonics in distributing southern marine taxa. Despite confident panbiogeographic claims to the contrary, molecular and ecological studies of buoyant macroalgae, such as Macrocystis, indicate that dispersal predominates. Ironically, some of the better supported evidence for marine vicariance in southern waters has little or nothing to do with plate tectonics. Rather, it involves far more localized and recent vicariant models, such as the isolating effect of the Bassian Isthmus during Pleistocene low sea‐level stands (Nerita). Main conclusions Recent phylogeographic studies of southern marine taxa (e.g. Diloma and Parvulastra) imply that passive rafting cannot be ignored as an important mechanism of long‐distance dispersal. I outline a new direction for southern hemisphere phylogeography, involving genetic analyses of bull‐kelp (Durvillaea) and its associated holdfast invertebrate communities.     

Integrating coalescent and ecological niche modeling in comparative phylogeography

Understanding the factors that contribute to the formation of population genetic structure is a central goal of phylogeographic research, but achieving this goal can be complicated by the stochastic variance inherent to genetic processes. Statistical approaches to testing phylogeographic hypotheses accommodate this stochasticity by evaluating competing models of putative historical population structure, often by simulating null distributions of the expected variance. The effectiveness of these tests depends on the biological realism of the models. Information from the fossil record can aid in reconstructing the historical distributions of some taxa. However, for the majority of taxa, which lack sufficient fossils, paleodistributional modeling can provide valuable spatial-geographic data concerning ancestral distributions. Paleodistributional models are generated by projecting ecological niche models, which predict the current distribution of each species, onto a model of past climatic conditions. Here, we generate paleodistributional models describing the suitable habitat during the last glacial maximum for lineages from the mesic forests of the Pacific Northwest of North America, and use these models to generate alternative phylogeographic hypotheses. Coalescent simulations are then used to test these hypotheses to improve our understanding of the historical events that promoted the formation of population genetic structure in this ecosystem. Results from Pacific Northwest mesic forest organisms demonstrate the utility of these combined approaches. Paleodistribution models and population genetic structure are congruent across three amphibian lineages, suggesting that they have responded in a concerted manner to environmental change. Two other species, a willow and a water vole, despite being currently codistributed and having similar population genetic structure, were predicted by the paleodistributional model to have had markedly different distributions during the last glacial maximum. This suggests that congruent phylogeographic patterns can arise from incongruent ancestral distributions. Paleodistributional models introduce a much-needed spatial-geographic perspective to statistical phylogeography. In conjunction with coalescent models of population genetic structure, they have the potential to improve our understanding of the factors that promote population divergence and ultimately produce regional patterns of biodiversity.     

Differences in Quaternary co-divergence reveals community-wide diversification in the mountains of southwest China varied among species

The mountains of southwest China (MSWC) is a biodiversity hotspot with highly complex and unusual terrain. However, with the majority of studies focusing on the biogeographic consequences of massive mountain building, the Quaternary legacy of biodiversity for the MSWC has long been overlooked. Here, we took a statistical comparative phylogeography approach to examine factors that shaped community-wide diversification. With data from 30 vertebrate species, the results reveal spatially concordant genetic structure, and temporally clustered co-divergence events associated with river barriers during severe glacial cycles. This indicates the importance of riverine barriers in the phylogeographic history of the MSWC vertebrate community. We conclude that the repeated glacial cycles are associated with co-divergences that are themselves structured by the heterogeneity of the montane landscape of the MSWC. This orderly process of diversification has profound implications for conservation by highlighting the relative independence of different geographical areas in which some, but not all species in communities have responded similarly to climate change and calls for further comparative phylogeographic investigations to reveal the connection between biological traits and divergence pulses in this biodiversity hotspot.     

A parasite-driven wedge: infectious diseases may explain language and other biodiversity

Parasite–host coevolutionary races are spatially variable across species' or human cultural ranges. Assortative sociality, biased toward local conspecifics, and limited dispersal (philopatry) in humans and other organisms can be adaptive through reduced contact with dangerous contagions harbored by distant/non-local conspecifics. These factors can generate cultural or population divergence. Thus, parasites are like a wedge driving groups apart through their effective creation of anticontagion behaviors. If this proposition is correct, then biological diversity should positively correlate with parasite diversity. Here we show that the worldwide distribution of indigenous human language diversity, a form of biodiversity, is strongly, positively related to human parasite diversity indicative of a legacy of parasite-mediated diversification. The significant pattern remains when potential confounds are removed. The pattern too is seen in each of the six world regions and is not confounded by regional differences in their history of colonization and conquest. We hypothesize that variation in limited dispersal and assortative sociality with conspecifics in response to the worldwide spatial variation in pathogen diversity provides a fundamental mechanism of population divergence explaining many important aspects of the geographic patterns of biodiversity. This hypothesis has broad implications for a diversity of research topics including language diversity, cultural evolution, speciation, phylogeny and biogeography.     

What has become of the refugia hypothesis to explain biological diversity in Amazonia?

The spatial distribution of biodiversity and related processes is the core of Biogeography. Amazonia is the world's most diverse rainforest and the primary source of diversity to several Neotropical regions. The origins of such diversity continue to be an unresolved question in evolutionary biology. Among many competing hypotheses to explain the evolution of the Amazonian biodiversity, one stands out as the most influential: the refugia hypothesis by Jürgen Haffer. Here, we provide a chronological overview on how the refugia hypothesis evolved over the decades and how the criticism from different fields affected its acceptance. We conclude that the refugia hypothesis alone cannot explain the diversification of the complex Amazonian diversity, and perhaps it was not the most important diversification mechanism. However, the debate provoked by refugia has produced a great amount of knowledge on Amazonian climatic, geological, and evolutionary processes, as well as on species distributions, movements, and history.     

Evolutionary origins of the eastern North American–Mesoamerican floristic disjunction: Current status and future prospects

Biogeographic disjunction patterns, where multiple taxa are shared between isolated geographic areas, represent excellent systems for investigating the historical assembly of modern biotas and fundamental biological processes such as speciation, diversification, niche evolution, and evolutionary responses to climate change. Studies on plant genera disjunct across the northern hemisphere, particularly between eastern North America (ENA) and eastern Asia (EAS), have yielded tremendous insight on the geologic history and assembly of rich temperate floras. However, one of the most prevalent disjunction patterns involving ENA forests has been largely overlooked: that of taxa disjunct between ENA and cloud forests of Mesoamerica (MAM), with examples including Acer saccharum, Liquidambar styraciflua, Cercis canadensis, Fagus grandifolia, and Epifagus virginiana. Despite the remarkable nature of this disjunction pattern, which has been recognized for over 75 years, there have been few recent efforts to empirically examine its evolutionary and ecological origins. Here I synthesize previous systematic, paleobotanical, phylogenetic, and phylogeographic studies to establish what is known about this disjunction pattern to provide a roadmap for future research. I argue that this disjunction pattern, and the evolution and fossil record of the Mexican flora more broadly, represents a key missing piece in the broader puzzle of northern hemisphere biogeography. I also suggest that the ENA–MAM disjunction represents an excellent system for examining fundamental questions about how traits and life history strategies mediate plant evolutionary responses to climate change and for predicting how broadleaf temperate forests will respond to the ongoing climatic pressures of the Anthropocene.